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Quantitative Ecological Genetics of Biotic Interaction

I am interested in how genetic variation shapes, and is shaped by, biotic interactions. To analyze quantitative genetic variation in complex ecological traits, my research employs cutting-edge tools from computational biology and functional genomics. Currently, I am working on plant-herbivore interactions, but other projects involving biotic interactions are also welcome.
Keywords: Ecology, Plant-insect interaction, Genetics of complex traits

Recent projects

1. Plant Neighborhood Effects and the Maintenance of Polymorphism

Herbivory risk depends on neighboring plants as well as plants’ own traits. Such neighbor effects can exert frequency-dependent selection on plant defense when they occur among plant genotypes within a species (reviewed by Sato 2018 Plant Species Biology). My PhD study showed that the feeding preference of a leaf beetle mediated negative frequency-dependent selection on the GLABRA1-based trichome dimorphism of Arabidopsis halleri (Sato & Kudoh 2017 The American Naturalist; Sato et al. 2017 Functional Ecology).

Hairy Arabidopsis halleri (left) and larval Phaedon brassicae (right) from Plant Species Biology Vol. 33(2)

2. Quantitative Genetics of Plant Neighborhood Effects on Herbivory

Plant neighborhood effects are not always attributable to a single trait or gene. To dissect the genetic architecture of neighbor effects, I have developed new methods called “Neighbor GWAS” (Sato et al. 2021 Heredity) and “Neighbor QTL” (Sato et al. 2021 G3). These new methods are being applied to the analysis of quantitative trait variation in insect herbivory and communities on Arabidopsis thaliana accessions.

Field experiment using Arabidopsis thaliana accessions. Modified from Sato et al. (2021) Heredity

Preprint

1. Sato Y*, Shimizu-Inatsugi R, Takeda K, Schmid B, Nagano AJ*, Shimizu KK*. (2023) Genome-wide neighbor effects predict genotype pairs that reduce herbivory in mixed planting. bioRxiv https://doi.org/10.1101/2023.05.19.541411

Peer-reviewed articles

1. Stockenhuber R, Akiyama R, Tissot N, Milosavljevic S, Yamazaki M, Wyler M, Arongaus AB, Podolec R, Sato Y, Widmer A, Ulm R*, Shimizu KK*. (2023) The UV RESISTANCE LOCUS 8-mediated UV-B response is required alongside CRYPTOCHROME1 for plant survival in sunlight under field conditions. Plant and Cell Physiology https://doi.org/10.1093/pcp/pcad113

2. Xu C^†, Sato Y^†*, Yamazaki M, Brasser M, Barbour MA, Bascompte J, Shimizu KK*. (2023) Genome-wide association study of aphid abundance highlights a locus affecting plant growth and flowering in Arabidopsis thaliana. Royal Society Open Science 10:230399. https://doi.org/10.1098/rsos.230399

3. Sato Y*, Takahashi Y, Xu C, Shimizu KK*. (2023) Detecting frequency-dependent selection through the effects of genotype similarity on fitness components. Evolution 77:1145–1157. https://doi.org/10.1093/evolut/qpad028 [Vignette]

4. Shimizu-Inatsugi R*, Morishima A, Mourato B, Shimizu KK, Sato Y. (2023) Phenotypic variation of a new synthetic allotetraploid Arabidopsis kamchatica enhanced in natural environment. Frontiers in Plant Science 13:1058522 https://doi.org/10.3389/fpls.2022.1058522

5. Takimoto H^†*, Sato Y^†, Nagano AJ, Shimizu KK, Kanagawa A. (2021) Using a two-stage convolutional neural network to rapidly identify tiny herbivorous beetles in the field. Ecological Informatics 66:101466 https://doi.org/10.1016/j.ecoinf.2021.101466

6. Sato Y, Yamamoto E, Shimizu KK*, Nagano AJ*. (2021) Neighbor GWAS: incorporating neighbor genotypic identity into genome-wide association studies of field herbivory. Heredity 126(4):597–614. https://doi.org/10.1038/s41437-020-00401-w [R package]

7. Sato Y^†*, Takeda K^†, Nagano AJ*. (2021) Neighbor QTL: an interval mapping method for quantitative trait loci underlying plant neighborhood effects. G3; Genes|Genomes|Genetics 11(2):jkab017. https://doi.org/10.1093/g3journal/jkab017 [R package]

8. Shimizu-Inatsugi R*, Milosavljevic S, Shimizu KK, Schaepman-Strub G, Tanoi K, Sato Y. (2021) Metal accumulation and its effect on leaf herbivory in an allopolyploid species Arabidopsis kamchatica inherited from a diploid hyperaccumulator A. halleri. Plant Species Biology 36(2):208–217. https://doi.org/10.1111/1442-1984.12304

9. Sato Y, Tezuka A, Kashima M, Deguchi A, Shimizu-Inatsugi R, Yamazaki M, Shimizu KK*, Nagano AJ*. (2019) Transcriptional variation in glucosinolate biosynthetic genes and inducible responses to aphid herbivory on field-grown Arabidopsis thaliana. Frontiers in Genetics 10:787. https://doi.org/10.3389/fgene.2019.00787

10. Sato Y, Shimizu-Inatsugi R, Yamazaki M, Shimizu KK*, Nagano AJ*. (2019) Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana. BMC Plant Biology 19:163. https://doi.org/10.1186/s12870-019-1705-2

11. Nakadai R^†*, Hashimoto K^†, Iwasaki T, Sato Y. (2018) Geographical co-occurrence of butterfly species: the importance of niche filtering by host plant species. Oecologia 186(4):995–1005. https://doi.org/10.1007/s00442-018-4062-1

12. Sato Y^†*, Ito K^†, Kudoh H. (2017) Optimal foraging by herbivores maintains polymorphism in defence in a natural plant population. Functional Ecology 31(12):2233-2243. https://doi.org/10.1111/1365-2435.12937 [postprint]

13. Sato Y*, Kudoh H. (2017) Herbivore-mediated interaction promotes the maintenance of trichome dimorphism through negative frequency-dependent selection. The American Naturalist 190(3):E67-E77. https://doi.org/10.1086/692603 [PDF]

14. Sato Y*, Kudoh H. (2017) Fine-scale frequency differentiation along a herbivory gradient in the trichome dimorphism of a wild Arabidopsis. Ecology and Evolution 7(7):2133-2141. https://doi.org/10.1002/ece3.2830

15. Sato Y*, Kudoh H. (2016) Presence of substitute diets alters plant resistance to specialist and generalist herbivores: a meta-analysis. Ecosphere 7(11):e01446 https://doi.org/10.1002/ecs2.1446

16. Sato Y*, Kudoh H. (2016) Associational effects against a leaf beetle mediate a minority advantage in defense and growth between hairy and glabrous plants. Evolutionary Ecology 30(1):137-154. https://doi.org/10.1007/s10682-015-9809-0 [postprint]

17. Sato Y*, Sato S. (2015) Spring temperature predicts the long-term molting phenology of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata (Hemiptera: Cicadidae). Annals of the Entomological Society of America 108(4):494-500. https://doi.org/10.1093/aesa/sav036 [postprint]

18. Sato Y*, Kudoh H. (2015) Tests of associational defence provided by hairy plants for glabrous plants of Arabidopsis halleri subsp. gemmifera against insect herbivores. Ecological Entomology 40(3):269-279. https://doi.org/10.1111/een.12179 [postprint]

19. Sato Y, Kudoh H*. (2014) Fine-scale genetic differentiation of a temperate herb: relevance of local environments and demographic change. AoB PLANTS 6:plu070. https://doi.org/10.1093/aobpla/plu070

20. Sato Y*, Kawagoe T, Sawada Y, Hirai MY, Kudoh H. (2014) Frequency-dependent herbivory by a leaf beetle, Phaedon brassicae, on hairy and glabrous plants of Arabidopsis halleri subsp. gemmifera. Evolutionary Ecology 28(3):545-559. https://doi.org/10.1007/s10682-013-9686-3 [postprint]

21. Sato Y*, Kudoh H. (2013) Relative strength of phenotypic selection on the height and number of flowering-stalks in the rosette annual Cardamine hirsuta (Brassicaceae). Journal of Ecology and Environment 36(3):151-158. https://doi.org/10.5141/ecoenv.2013.151

22. Sato Y*, Takakura KI, Nishida S, Nishida T. (2013) Dominant occurrence of cleistogamous flowers of Lamium amplexicaule in relation to the nearby presence of an alien congener L. purpureum. ISRN Ecology Article ID:476862. http://dx.doi.org/10.1155/2013/476862

Peer-reviewed monographs/reviews

1. Sato Y*. (2018) Associational effects and the maintenance of polymorphism in plant defense against herbivores: review and evidence. Plant Species Biology 33(2):91-108. https://doi.org/10.1111/1442-1984.12201 [postprint]

2. Sakata Y*, Sato Y. (2017) Evolutionary ecology of plant defense: integrating different spatial scales within and among species (in Japanese). Japanese Journal of Ecology 67(3):287-306. https://doi.org/10.18960/seitai.67.3_287

Peer-reviewed conference proceedings

1. Kuzuhara H, Takimoto H, Sato Y, Kanagawa A. (2020) Insect pest detection and identification method based on deep learning for realizing a pest control system. Proceedings of the Society of Instrument and Control Engineers (SICE) Annual Conference 2020. pp. 709–714. https://doi.org/10.23919/SICE48898.2020.9240458

Books

1. Sato Y, Muranaka T. (eds). (2023) Trans-Scale Biology of Plants: Integrating genomics, phenomics, and ecology to unveil biodiversity (in Japanese). Species Biology Series, Bun-ichi Sogo Shuppan, Tokyo, Japan. ISBN: 978-4-8299-6210-7.

Conference contributions

1. Sato Y, Shimizu-Inatsugi R, Takeda K, Nagano AJ, Shimizu KK. Genome-wide neighbor effects predict genotype pairs reducing herbivory in mixed planting. Biodiversity Convention - From Science to Implementation, Monte Verita, Ascona, Switzerland (27 June 2023, talk)

2. Sato Y, Shimizu-Inatsugi R, Takeda K, Nagano AJ, Shimizu KK. Keystone pairs of Arabidopsis accessions increase plant resistance to field herbivory. In Concurrent 15: Arabidopsis relatives from laboratories to natural fields (organized by Prof. K.K. Shimizu and H. Kudoh). The 33rd International Conference on Arabidopsis Research (ICAR2023), Chiba, Japan (7 June 2023, talk)

3. Sato Y, Shimizu-Inatsugi R, Takeda K, Nagano AJ, Shimizu KK. Keystone genotype pairs increase plant resistance to herbivory. Gordon Research Conference: Plant-Herbivore Interaction 2023, Ventura, CA, USA (2 March 2023, poster)

4. Sato Y, Shimizu-Inatsugi R, Takeda K, Nagano AJ, Shimizu KK. Keystone genotype pairs increase population-level resistance to herbivory. SwissPLANT 2023 Symposium, Les Diablerets, Switzerland (23 January 2023, talk)

5. Sato Y, Shimizu-Inatsugi R, Nagano AJ, Shimizu KK. Neighbor GWAS: incorporating neighbor genotypic identity in genome-wide association study of field-grown Arabidopsis thaliana. ‘From place to space - Tracing the spatial dimension of plant sciences’ by Plant Science Center Symposium 2022, P30, ETH Zurich, Switzerland (7 December 2022, poster)

6. Sato Y, Takahashi Y, Xu C, Shimizu KK. Detecting frequency-dependent selection using a genetic marker regression of fitness components. In: S24 ‘Progress and Prospects in Adaptation Genomics’. The 2022 Congress of the European Society for Evolutionary Biology, Prague, Czech Republic (18 August 2022, reviewed talk)

7. Sato Y, Nagano AJ, Shimizu KK. Genomics of within-species mixed planting against insect herbivores. In: MON3-b ‘From the species to the individual: investigating plant diversity on the scale that matters most’ (organized by Drs. P. Villa and M.C. Schuman). World Biodiversity Forum 2022, Davos, Switzerland. (29 June 2022, reviewed talk) https://www.worldbiodiversityforum.org/

8. Kuzuhara H, Takimoto H, Sato Y, Kanagawa A. Insect pest detection and identification method based on deep learning for realizing a pest control system. The Society of Instrument and Control Engineers (SICE) Annual Conference 2020. Chiang Mai, Thailand [changed into an online meeting due to COVID-19] (25 September 2020, talk)

9. Sato Y. Using personal legacy data to reveal the molting phenology of Japanese cicadas. In: S19 ‘Ongoing Cicada Research in East Asia’ (organized by Prof. J. Yikweon), The 8th EAFES International Congress, Nagoya, Japan (April 2018, invited talk)

Besides 7 English posters and 35 Japanese contributions (4 invited talks, 10 talks, and 21 posters)

Yasuhiro Sato

During my childhood, I collected nymphal shells of Japanese cicadas over the course of ten years (Sato & Sato 2015). This early experience sparked my interest in ecology later in life.

I received my bachelor’s, master’s, and doctoral degrees from Kyoto University in Japan. My undergraduate studies were completed in 2011 at the Laboratory of Insect Ecology, and I received my PhD in 2016 from the Laboratory of Plant Molecular Ecology (Kudoh Group) at the Center for Ecological Research. My experience in entomology and botany sparked my interest in plant-insect interactions.

After earning my PhD, I completed two postdoctoral positions at Ryukoku University in Japan: one as an independent postdoctoral fellow of the Japan Society for the Promotion of Science (JSPS) from 2016 to 2017 and one as a junior group leader of the Precursory Research for Embryonic Science and Technology (PRESTO) program of the Japan Science and Technology Agency (JST) from 2017 to 2021. During my five years at the Laboratory of Information Biology (Nagano Group), I acquired skills in plant bioinformatics and functional genomics.

During my first postdoctoral position, I began collaborating with the Evolutionary and Ecological Genomics Group (Shimizu Laboratory) at the University of Zurich in Switzerland as an affiliated member of the University Research Priority Program of Global Change and Biodiversity (URPP GCB). After completing the JST PRESTO program in Japan, I moved to Switzerland and joined the Department of Evolutionary Biology and Environmental Studies at the University of Zurich as a senior research and teaching assistant in 2021.

Education

• 23 March 2016. PhD in Science, Center for Ecological Research, Graduate School of Science, Kyoto University, Japan (supervisor: Prof. Dr. Hiroshi Kudoh) [PhD defended on 28 January 2016]
• 25 March 2013. MSc in Science, Center for Ecological Research, Graduate School of Science, Kyoto University, Japan (supervisor: Prof. Dr. Hiroshi Kudoh)
• 24 March 2011. BSc in Agriculture, Laboratory of Insect Ecology, Faculty of Agriculture, Kyoto University, Japan (supervisor: Assistant Prof. Dr. Takayoshi Nishida)

Research position

• 2021.04 - Present: Oberassistent (Senior research and teaching assistant), Department of Evolutionary Biology and Environmental Studies, University of Zurich, Switzerland (Evolutionary and Ecological Genomics Group)
  
• 2017.10 - Present: Guest researcher of Research Institute for Food and Agriculture, Ryukoku University, Japan
  
• 2017.08 - Present: Affiliated member of University Research Priority Program Global Change and Biodiversity (URPP GCB), University of Zurich, Switzerland
  
• 2017.10 - 2021.03: Fixed-term group leader of Precursory Research for Embryonic Science and Technology (PRESTO) project of Japan Science and Technology Agency (JST), Japan
• 2016.04 - 2020.03: Affiliated scientist of Center for Ecological Research, Kyoto University
• 2016.04 - 2017.09: Independent Postdoctoral Fellowship of Japan Society for the Promotion of Science (JSPS), Japan (advisor: Assoc. Prof. Atsushi J. Nagano)
• 2015.04 - 2016.03: Research Fellowship for PhD students (DC2), JSPS, Japan
• 2013.06 - 2014.03: Research assistant of Center for Ecological Research, Kyoto University, Japan

Teaching experience

• 2021.09 - Present: BIO373. Next Generation Sequencing for Evolutionary Functional Genomics, University of Zurich, Switzerland (Block course management, Co-instructor)
  
• 2022.05: BIO334. Practical Bioinformatics, University of Zurich, Switzerland (Co-instructor)
  
• 2019.04 - 2019.05: External Lecturer of Basic Genetics, Faculty of Agriculture, Ryukoku University, Japan (Co-instructor)
  
• 2018.07 - 2018.08: International Biology Undergraduate Summer School (BUSS) 2018, University of Zurich, Switzerland (Co-supervisor)
  
• 2017.07 - 2017.08: BIO378. Research Practical in Evolutionary Biology and Systematics, University of Zurich, Switzerland (Co-supervisor)
  
• 2013.09 - 2015.01: External Teaching Assistant of Basic Programming, Faculty of Science and Technology, Ryukoku University, Japan

Awards

1. Inoue Research Award for Early-career Scientists, Inoue Foundation for Science (2018)
2. Kataoka Award, The Society for the Study of Species Biology (2016)
3. Ikushi Prize, Japan Society for the Promotion of Science (2016)

Grants

1. JSPS Grants-in-Aid for Early-career Scientists (2023-2027, 3,600,000JPY as Principal Investigator)
2. JSPS Grants-in-Aid for Early-career Scientists (2020-2023, 3,200,000JPY as Principal Investigator)
3. JST Precursory Research for Embryonic Science and Technology (PRESTO) (2017-2021, 40,000,000JPY as Principal Investigator)
4. JSPS Research Fellowships for Early-career Scientists (PD) (2016-2017, 2,700,000JPY)
5. JSPS Research Fellowships for Early-career Scientists (DC2) (2015-2016, 1,200,000JPY)
6. JASSO Scholarship (2011-2015, 4,000,000JPY)

Panels and boards

• 2019.01 - Present: Editorial board member of the Society for the Study of Species Biology, Japan
  
• 2019.09 - 2021.12: Reviewing editor of Journal of Evolutionary Biology

Affiliated academic societies

• 2010 - Present: Society for the Study of Species Biology
  
• 2012 - Present: Ecological Society of Japan
  
• 2017 - Present: Japanese Society of Plant Physiologists
  
• 2017 - Permanent: American Society of Naturalists
  
• 2020 - Present: European Society for Evolutionary Biology

Reviewer activity

• see ResearcherID verified via Publons

^{(c) 2013- Yasuhiro Sato, All rights reserved.}